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From neural plate to cortical arousal-a neuronal network theory of sleep derived from in vitro "model" systems for primordial patterns of spontaneous bioelectric activity in the vertebrate central nervous system.

Corner MA - Brain Sci (2013)

Bottom Line: Such rhythmically modulated phasic bursts were next discovered to be a general feature of developing neural networks and, largely on the basis of experimental interventions in cultured neural tissues, to contribute significantly to their morpho-physiological maturation.In contrast, a late onto- and phylogenetic aspect of sleep, viz., the intermittent "paradoxical" activation of the forebrain so as to mimic waking activity, is much less well understood as regards its contribution to brain development.Some recent findings dealing with this question by means of cholinergically induced "aroused" firing patterns in developing neocortical cell cultures, followed by quantitative electrophysiological assays of immediate and longterm sequelae, will be discussed in connection with their putative implications for sleep ontogeny.

View Article: PubMed Central - PubMed

Affiliation: Netherlands Institute for Brain Research, Amsterdam, 1071-TC, The Netherlands. m.corner@hccnet.nl.

ABSTRACT
In the early 1960s intrinsically generated widespread neuronal discharges were discovered to be the basis for the earliest motor behavior throughout the animal kingdom. The pattern generating system is in fact programmed into the developing nervous system, in a regionally specific manner, already at the early neural plate stage. Such rhythmically modulated phasic bursts were next discovered to be a general feature of developing neural networks and, largely on the basis of experimental interventions in cultured neural tissues, to contribute significantly to their morpho-physiological maturation. In particular, the level of spontaneous synchronized bursting is homeostatically regulated, and has the effect of constraining the development of excessive network excitability. After birth or hatching, this "slow-wave" activity pattern becomes sporadically suppressed in favor of sensory oriented "waking" behaviors better adapted to dealing with environmental contingencies. It nevertheless reappears periodically as "sleep" at several species-specific points in the diurnal/nocturnal cycle. Although this "default" behavior pattern evolves with development, its essential features are preserved throughout the life cycle, and are based upon a few simple mechanisms which can be both experimentally demonstrated and simulated by computer modeling. In contrast, a late onto- and phylogenetic aspect of sleep, viz., the intermittent "paradoxical" activation of the forebrain so as to mimic waking activity, is much less well understood as regards its contribution to brain development. Some recent findings dealing with this question by means of cholinergically induced "aroused" firing patterns in developing neocortical cell cultures, followed by quantitative electrophysiological assays of immediate and longterm sequelae, will be discussed in connection with their putative implications for sleep ontogeny.

No MeSH data available.


Related in: MedlinePlus

Comparison between control cultures (blue: n = 6) and overnight TTX (20 μM) pre-treated cultures (red: n = 7) for selected parameters of spontaneous activity. MFR = mean firing rate; burst intensity = intraburst firing rate; inverse ratio = the proportion of spikes falling outside bursts (interspike interval detection criterion for bursts ≤100 ms). All values were normalized with respect to the mean level in the 2-h period prior to administering 20 μM carbachol (for ~20 h), followed by ~20 h of washout. The individual means at each time point were then used to calculate a grand mean for each group, with error bars indicating the SEM. (For examples of actual polyneuronal firing patterns throughout a representative experiment, see [13]).
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brainsci-03-00800-f008: Comparison between control cultures (blue: n = 6) and overnight TTX (20 μM) pre-treated cultures (red: n = 7) for selected parameters of spontaneous activity. MFR = mean firing rate; burst intensity = intraburst firing rate; inverse ratio = the proportion of spikes falling outside bursts (interspike interval detection criterion for bursts ≤100 ms). All values were normalized with respect to the mean level in the 2-h period prior to administering 20 μM carbachol (for ~20 h), followed by ~20 h of washout. The individual means at each time point were then used to calculate a grand mean for each group, with error bars indicating the SEM. (For examples of actual polyneuronal firing patterns throughout a representative experiment, see [13]).

Mentions: Transfer to a carbachol containing medium almost immediately led to a strong decrease in synchronous firing [14] as well as causing the detected bursts of activity [54,55] to become significantly longer and less intense, while mean firing rates and the “inverse burst ratio” (i.e., the proportion of “background” spikes falling between successive spike clusters) showed a clear cut trend towards enhancement (Figure 8). Only the inverse burst ratio was obviously affected by prior suppression of spontaneous spiking by means of tetrodotoxin (TTX), a treatment which neutralized carbachol”s subsequent acute effect (p < 0.05: Fisher exact-p test). The “burst index”, a measure of fluctuating activity levels over a period of several minutes [89], showed little or no change upon transfer to carbachol, whether or not spike discharges had been present in the preceding 24 h period (Figure 9).


From neural plate to cortical arousal-a neuronal network theory of sleep derived from in vitro "model" systems for primordial patterns of spontaneous bioelectric activity in the vertebrate central nervous system.

Corner MA - Brain Sci (2013)

Comparison between control cultures (blue: n = 6) and overnight TTX (20 μM) pre-treated cultures (red: n = 7) for selected parameters of spontaneous activity. MFR = mean firing rate; burst intensity = intraburst firing rate; inverse ratio = the proportion of spikes falling outside bursts (interspike interval detection criterion for bursts ≤100 ms). All values were normalized with respect to the mean level in the 2-h period prior to administering 20 μM carbachol (for ~20 h), followed by ~20 h of washout. The individual means at each time point were then used to calculate a grand mean for each group, with error bars indicating the SEM. (For examples of actual polyneuronal firing patterns throughout a representative experiment, see [13]).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4061857&req=5

brainsci-03-00800-f008: Comparison between control cultures (blue: n = 6) and overnight TTX (20 μM) pre-treated cultures (red: n = 7) for selected parameters of spontaneous activity. MFR = mean firing rate; burst intensity = intraburst firing rate; inverse ratio = the proportion of spikes falling outside bursts (interspike interval detection criterion for bursts ≤100 ms). All values were normalized with respect to the mean level in the 2-h period prior to administering 20 μM carbachol (for ~20 h), followed by ~20 h of washout. The individual means at each time point were then used to calculate a grand mean for each group, with error bars indicating the SEM. (For examples of actual polyneuronal firing patterns throughout a representative experiment, see [13]).
Mentions: Transfer to a carbachol containing medium almost immediately led to a strong decrease in synchronous firing [14] as well as causing the detected bursts of activity [54,55] to become significantly longer and less intense, while mean firing rates and the “inverse burst ratio” (i.e., the proportion of “background” spikes falling between successive spike clusters) showed a clear cut trend towards enhancement (Figure 8). Only the inverse burst ratio was obviously affected by prior suppression of spontaneous spiking by means of tetrodotoxin (TTX), a treatment which neutralized carbachol”s subsequent acute effect (p < 0.05: Fisher exact-p test). The “burst index”, a measure of fluctuating activity levels over a period of several minutes [89], showed little or no change upon transfer to carbachol, whether or not spike discharges had been present in the preceding 24 h period (Figure 9).

Bottom Line: Such rhythmically modulated phasic bursts were next discovered to be a general feature of developing neural networks and, largely on the basis of experimental interventions in cultured neural tissues, to contribute significantly to their morpho-physiological maturation.In contrast, a late onto- and phylogenetic aspect of sleep, viz., the intermittent "paradoxical" activation of the forebrain so as to mimic waking activity, is much less well understood as regards its contribution to brain development.Some recent findings dealing with this question by means of cholinergically induced "aroused" firing patterns in developing neocortical cell cultures, followed by quantitative electrophysiological assays of immediate and longterm sequelae, will be discussed in connection with their putative implications for sleep ontogeny.

View Article: PubMed Central - PubMed

Affiliation: Netherlands Institute for Brain Research, Amsterdam, 1071-TC, The Netherlands. m.corner@hccnet.nl.

ABSTRACT
In the early 1960s intrinsically generated widespread neuronal discharges were discovered to be the basis for the earliest motor behavior throughout the animal kingdom. The pattern generating system is in fact programmed into the developing nervous system, in a regionally specific manner, already at the early neural plate stage. Such rhythmically modulated phasic bursts were next discovered to be a general feature of developing neural networks and, largely on the basis of experimental interventions in cultured neural tissues, to contribute significantly to their morpho-physiological maturation. In particular, the level of spontaneous synchronized bursting is homeostatically regulated, and has the effect of constraining the development of excessive network excitability. After birth or hatching, this "slow-wave" activity pattern becomes sporadically suppressed in favor of sensory oriented "waking" behaviors better adapted to dealing with environmental contingencies. It nevertheless reappears periodically as "sleep" at several species-specific points in the diurnal/nocturnal cycle. Although this "default" behavior pattern evolves with development, its essential features are preserved throughout the life cycle, and are based upon a few simple mechanisms which can be both experimentally demonstrated and simulated by computer modeling. In contrast, a late onto- and phylogenetic aspect of sleep, viz., the intermittent "paradoxical" activation of the forebrain so as to mimic waking activity, is much less well understood as regards its contribution to brain development. Some recent findings dealing with this question by means of cholinergically induced "aroused" firing patterns in developing neocortical cell cultures, followed by quantitative electrophysiological assays of immediate and longterm sequelae, will be discussed in connection with their putative implications for sleep ontogeny.

No MeSH data available.


Related in: MedlinePlus